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VOLUME XXXIX NUMBER
GAMETOPHYTES AND EMBRYO OF TORREYA TAXI-
CONTRIBUTIONS FROM THE HULL BOTANICAL LABORATORY.
John M. Coulter and W. J. G. Land.
(WITH PLATES A, I, II, III)
Torreya taxijolia Arnott 1 occurs in a narrow belt along the eastern
side of the Apalachicola River, extending from the southern boundary
of Georgia for about thirty miles southward (1). In April 1904 this
region was visited by H. C. Cowles of this laboratory, among whose
notes the following are of interest in this connection :
My visit was to the northernmost colony, west of Chattahoochee village, and
close to the Georgia line. The distribution lines on Chapman's map (1) would
lead one to suppose that the tree is xerophytic and frequents the steep and dry
eastern bluffs. I was much surprised to find that it was confined (in the Chatta-
hoochee station at least) to the extremely mesophytic slopes of ravines, growing
exclusively in the shade of trees, and in places that are continually moist, prefer-
ably on slopes facing north. The northern and southern known limits of the
tree are only about thirty miles apart, and the east-west range is much less.
Furthermore, on account of the great economic value of the wood, and the
familiarity of the tree to all the inhabitants of the region, the likelihood of finding
other areas is very slight.
It is associated with a remarkable and somewhat extensive group of northern
mesophytic plants, and the conclusion is irresistible that Torreya is a northern
plant of the most pronounced mesophytic tendencies, and to be associated with
1 Unfortunately, Torreya was used at least three times as a generic name, in as
many families, before 1838, the date of the publication of Torreya Arnott. Hence
Arnott' s genus has been replaced by Tumion Raf., and our species becomes Tumion
taxijolia Greene. In the present paper, however, the more familiar name is used for
162 BOTANICAL GAZETTE [maech
such forms as the beech-maple-hemlock forms of our northern woods, our most
mesophytic type of association. Probably it never becomes a large tree, although
farmers always cut the trees as soon as they become at all usable. Rarely were
any found over 3o cm in diameter or more than 9 to i2 m high. It has remark-
able capacity for vegetative reproduction, almost equaling the redwood in this
respect. Many suckers issue from cut stumps, and even from fallen trunks;
even rotten stumps show vigorous suckers, and it seems to be as tenacious of life
as the poplar. Staminate trees appear to be the more numerous; however,
when in blossom they are far more conspicuous than are the pistillate trees, and
the conclusion as to proportion may not hold.
Cowles secured collections of staminate and ovulate material
April 4 and 5, and arranged for subsequent collections to be sent to
the laboratory. These collections were made at intervals of approxi-
mately two weeks up to October 21. The strobilus-bearing twigs
were packed in damp cotton in tightly closed tin buckets and reached
the laboratory in good condition in about five days. The length of
the intervals between collections and between collecting and killing
has prevented so close a series as is desirable at certain stages, but
the gymnosperm periods are so long that a fair outline of morpho-
logical events was secured.
Strobili. — The staminate strobili occur in the axils of leaves of
young shoots. Their appearance in October, on a shoot of the
same season, is shown in fig. 1. At this time they are small and
ovoid, solitary in the axil of each leaf, and by a curving of the short
peduncles are displayed along the under surface of the shoot. The
strobilus consists of a series of closely overlapping sterile bracts, in
four vertical rows, completely enveloping the tip of the axis bearing
numerous stamens. It is thus distinctly sterile below and fertile
above, the sporophylls continuing the spiral succession developed
by the bracts (figs. 6 and 7).
The young strobili were first observed in July, and at that time
no primordia of sporophylls were evident; but in August these were
beginning to appear. Fig. 7 is from a longitudinal section through
a strobilus at this period (August 12), showing the overlapping sterile
bracts and the beginning of stamineal primordia. A remarkable
development of the pith region of the axis below the staminate por-
1905] COULTER &> LAND—TORREYA TAXIFOLIA 163
tion of the strobilus, with its investing vascular cylinder, may be
observed, apparently an important storage region for the strobilus.
Stamens. — At the stage of the stamineal primordia observed
August 12, there is no evident differentiation of tissues (fig. 8), but
early in September the young sporangia become distinct, the sporo-
genous tissue being represented in each case by a single primary
sporogenous cell. At this stage the further development of the
young sporangia differs. Seven sporangia are seen in the primary
sporogenous cell stage, three adaxial and four abaxial (fig. 10),
radially arranged about the central axis as are the five or more spor-
angia in the allied Taxus. The four abaxial sporangia develop in
the usual way, and become the pendent abaxial sporangia character-
istic of Torreya. The three adaxial sporangia, however, do not
develop further, the primary sporogenous cell not dividing, and its
nucleus showing signs of disorganization (fig. 9). The disorganiza-
tion continues until it involves all the cells separating the three adaxial
sporangia, which are thus replaced by a single large flattened cavity,
which becomes a resin cavity. Intermediate stages were found in
which the three sporogenous regions were still distinct (fig. 10). In
fig. 11 (October 21) is shown a median longitudinal section through
a stamen, in which the large resin cavity is seen above and the nor-
mally developing sporogenous tissue below. As a result, the mature
stamen of Torreya is characterized by four abaxial sporangia and a
large adaxial resin cavity.
In one instance the two lateral sporangia were smaller than the
middle ones (fig. 10), suggesting a tendency to still greater reduction
in the number of sporangia. Accordingly Pinus Laricio was exam-
ined, and two resin cavities were found related to the two sporangia
exactly as the two lateral sporangia of Torreya are to the middle
ones ; and in early stages the tissue on the sites of these two resin cavi-
ties of Pinus resembles that of sporangia. It is interesting to note
that in T. californica Miss Robertson (8) found occasional stamens
bearing six or seven mature sporangia, indicating that in these cases
some or all of the usually abortive sporangia reached maturity.
There is evident a tendency to reduce the number of functioning
sporangia by abortion, a reduction that has proceeded farther in
Pinus than in Torreya; and in the latter farther than in Taxus. That
164 BOTANICAL GAZETTE [maech
the cavities formed by the breaking down of young sporogenous and
adjacent tissue should become resin cavities in conifers is to be
It was only in the abortive sporangia of Torreya that stages were
found indicating the history of the sporangium up to the primary
sporogenous cell stage. For example, from fig. g it seems evident
that there was a single hypodermal archesporial cell, which at this
stage had given rise to two layers of wall cells and a single primary
sporogenous cell. In the mature sporangium there are three or four
wall layers. The epidermis contains numerous stomata, and its
cells become prominent and have thickened walls. The sporangia
are bluntly four-angled from pressure, and the epidermal cells at
the angles are much larger than elsewhere.
Male gametophyte. — We secured no stages between the very
young sporangium and the shedding of the pollen, which occurs late
in March and early in April. Miss Robertson (8) has observed
the mother- cell stage and the formation of tetrads in T. calijomica.
In germination the microspore of T. taxijolia cuts off no prothallial
cell, a feature common to all the Coniferales except Podocarpeae
and Abieteae. After the first division the generative and tube cells
are distinct and separated by a very delicate wall or membrane.
The tube nucleus is sometimes spherical, but more often amoeboid
Early in April the binucleate pollen grains, rich in starch, were
found resting on the nucellus (fig. ig) ; and at the end of June micro-
pyles were found full of pollen grains, most of which had sent out no
tubes, but were still full of starch, nucleate, and apparently alive.
As fertilization occurs about the middle of August, active pollen
tubes occupy the sterile cap of the nucellus about four months, and
their behavior is exceedingly variable. They may advance towards
the embryo sac rapidly, reaching it at a very early stage, as early as
June 21, when the endosperm consists of only sixteen to sixty-four
parietally placed free nuclei (figs. 14 and 15); or they may advance
slowly, being found at all stages of progress at the same date. They
may advance so directly that the tube resembles a straight cleft
through the nucellar tissue to the sac, or they may pursue a remark-
ably devious course. In one case a tube passed directly half-way
1905] COULTER & LAND—TORREYA TAXIFOLIA 165
down the nucellar cap, then advanced spirally downward and out-
ward until it reached the peripheral cells of the nucellus, and after
destroying several of these it turned abruptly inward, penetrated the
nucellus at the level of the archegonium, crossed the top of the endo-
sperm, and discharged its contents into the archegonium on the farther
side. In another instance, such a pollen tube had entered the inner
integument and destroyed some of its cells before turning back into
the nucellus. It is very common for the pollen tube to push into the
sac at its free nuclear stage, making a deep invagination, often to the
middle; from this pocket the tube turns back again into the nucellus.
It is of interest to note in this connection that the usually solitary
archegonium is never centrally placed in the endosperm, and the
pollen tube enters the sac to one side of it (fig. 16).
In all the wanderings of the pollen tube, the body cell, stalk
nucleus, and tube nucleus are conspicuous. The division of the
generative cell was not observed, but that it occurs very early in
the development of the tube is evident. The body cell is relatively
very large, with a conspicuous nucleus and investing cytoplasm, and
was always found consorting closely with the stalk and tube nuclei
(figs. 13 and 14).
The division of the body cell just before fertilization results in
unequal male cells (fig. 23), almost exactly resembling those of Taxus.
It is not a case of the extrusion of one nucleus from the common
cytoplasm, as observed by Coker (2) in Podocarpus, but the cyto-
plasm is unequally divided, so that there are two distinct and naked
male cells very different in size. The whole cavity of the pollen
tube surrounding the cells and nuclei is rich in starch and other food
materials (fig. 13).
A consideration of the time involved in these various events shows
that a period of about fifteen months elapses between the first appear-
ance of the microsporangiate strobilus and fertilization, divided as
follows: June, first appearance of strobilus; August, first appearance
of stamineal primordia; September, distinct differentiation of spor-
angia; April, shedding of spores; August, fertilization. The stro-
bilus was first observed in July, but in such a condition that it must
have been evident in June, if not earlier. In comparing this schedule
with that given by Miss Robertson (8) for T. calijomica, it is evident
166 BOTANICAL GAZETTE [march
that the sporangium in both species passes the winter in the mother-
cell stage, but that the subsequent stages appear earlier in T. taxijolia
growing in its natural habitat than in T. califomica growing in Eng-
land. For example, in the latter case the reduction division takes
place about the time that T. taxijolia sheds its pollen, and pollination
in T. califomica does not seem to occur until late in May or early in
Strobili. — The ovulate strobili are borne in the axils of the lower
leaves of short young shoots (fig. 2). They usually occur in pairs
upon a very short axillary branch, usually one pair, frequently two
pairs, very rarely three pairs appearing upon a single shoot. A
cluster of two to six strobili, therefore, appears near the base of the
strobilus-bearing shoot, the upper pairs never maturing, usually
one and sometimes both strobili of the lowest pair producing the
large plum-like seeds (fig. j). The strobilus is a very simple one,
consisting of four enveloping bracts and a single terminal ovule with
two integuments (figs. 17 and 18), the outer one often called an arillus
because it ripens fleshy. The whole structure resembles a simple
ovulate flower with a perianth of four bracts, which perhaps deserve
to be called a perianth as much as the so-called perianth of Gnetales;
but it is none the less evident that they are the sterile bracts of a much
The strobili were first seen July 26, at which time the growing
point, enclosed by the bracts, was composed of entirely homogeneous
tissue, showing no differentiation as an ovule (fig. 17). No subse-
quent stages were found until April 7 (fig. 18), when the mother-cells
were in synapsis (fig. 20) ; and it seems probable that the winter was
passed in the mother-cell stage. At this time the integuments are
entirely free from the nucellus, appearing to arise from the base of
the ovule. Soon, however, extensive intercalary growth below the
mother-cell becomes evident, the ovule being greatly elongated and
broadened below, the original free nucellus with its integuments
forming only the tip. This growth continues throughout the season
of fertilization and the following one; and Oliver (6), who has
described this intercalary growth in T. nucifera, estimates that in
that species in the maturing seed the original nucellus with its free
1905] COULTER &• LAND—TORREYA TAXIFOLIA 167
integuments represents only one- twentieth of the entire length of the
seed. The characteristic structures of the integuments are con-
tinued as two distinct peripheral layers of this large mass of additional
tissue, and the tissue within these layers may be taken to represent
in a similar way the downward extension of the nucellus. It is this
additional nucellar tissue that the endosperm chiefly invades, giving
rise to the phenomenon of " rumination," to be described later.
Oliver (7) has also described fully the course of the vascular strands
in the ovule of certain species of Torreya, a description which seems
to serve as well for T. taxijolia.
Female gametophyte. — The mother-cell is solitary and with
no differentiation of a nutritive mechanism about it, such as appears
in connection with the " spongy tissue" of Pinus, and in all the
Pinaceae investigated. In Torreya it is directly in contact with the
cells that are resorbed, without any intervening digestive layer (fig.
20). Since this is true also of Podocarpus (2) and Taxus (10), it
suggests the possibility that Taxaceae in general may be character-
ized by the absence of a special digestive layer about the mother- cell.
The reduction division was not seen, but a more or less complete
tetrad is formed, as observed by Miss Robertson (8) also in T.
The germination of the megaspore begins with the usual free
nuclear division, the nuclei being in the parietal position when only
sixteen to thirty- two in number (figs. 14 and 15). The interior of
the sac contains cytoplasmic material, much less dense than the
cytoplasm of the parietal layer, and also some reserve food. In this
early few-nucleate stage of the endosperm there is always an appear-
ance suggesting that the sac has sent a beak-like projection, contain-
ing a nucleus, upwards into the nucellar tissue (fig. 15). After a
careful comparison of the position of this apparent projection in
reference to the surrounding parts with that of the megaspore, it
seems that the " projection" is the original site of the megaspore,
and that the appearance of a projection is due to the fact that the sac
has encroached almost exclusively upon the chalazal tissue. This
conspicuous beak, containing one of the parietal nuclei, often appears
close to the tip of an advancing pollen tube, and suggests a possible
explanation of the peculiar behavior ascribed to the archegonium
1 68 BOTANICAL GAZETTE [march
initial of Tumboa. Inasmuch as the archegonium initial of Torreya
often occupies this beak, the suggestion becomes still more pertinent
The formation of walls in the endosperm was not observed before
July i, and in several instances they did not appear for a month later.
When wall-formation began, repeated countings showed 256 free
nuclei, which seems to be a very common limit of free nuclear division
Since fertilization was observed August 12, it is evident that the
archegonium is developed very early in the history of the gameto-
phyte. In fact, as soon as the very small sac is filled with extremely
delicate tissue the archegonium initial becomes evident. It does not
seem possible for archegonia to appear any earlier, for the initials
are organized as soon as the free nuclear stage has passed. In
Torreva, therefore, nearly all of the endosperm, which becomes an
extensive tissue, develops after fertilization.
The single archegonium initial is always to one side of the central
axis (fig. 16), often occupying the "beak" referred to above, and so
projecting above the endosperm (fig. 21). A neck cell is cut off
and divides anticlinally, forming a two-celled neck (fig. 22), the
usual limit of neck-formation among gymnosperms. In fact, it is
only among Podocarpeae and Abieteae that a more extensive neck
is usually formed, consisting of more than one tier of cells, unless the
somewhat anomalous neck of Ephedra be included. The fact that
there is variation in the number of neck cells in the same form (two to
twenty-five in Podocarpus), and that as a rule necks are destroyed
as soon as formed by the growth of the central cell and pollen tube
(fig. 23), suggests that their extent depends somewhat upon the
approach of the pollen tube, which usually checks neck formation
early, but sometimes permits it to become more extensive. In T.
calijomica Miss Robertson (9) has found that the archegonia are
usually three in number, ranging from two to five, and that the necks
consist of four or six cells.
The central cell enlarges rapidly, no jacket-layer being evident
until after fertilization, and even then it is weakly organized (fig. 25).
The nucleus is spherical and lies near but not against the neck cells,
more nearly resembling an egg nucleus than in any gymnosperm
1905] COULTER fir- LAND—TORREYA TAXIFOLIA 169
we have observed (fig. 22). We could not detect the formation of a
ventral canal cell or nucleus, or anything that stood for such a struct-
ure at later stages. A ventral nucleus was expected, for a distinct
ventral canal cell among Coniferales seems to be restricted to the
Abieteae and does not always occur in them, and there seemed to be
no excuse in our preparations for missing it. We are fully aware
that all previous negative evidence as to the occurrence of at least a
ventral nucleus in archegonium-forming gymnosperms has proved
to be deceptive, but a study of the behavior of the central cell of
Torreya, from the formation of the neck cell to fertilization, not only
failed to show any indication of division but suggested that it may
not occur. In T. californica a spindle seen twice in the central cell
was interpreted by Miss Robertson (9) as representing the " cutting
off" of a ventral nucleus, but no other traces of it could be found.
In the single case in which two archegonia were observed, they
were at opposite sides of the gametophyte, with the tip of a pollen
tube between them.
At the time of fertilization the gametophyte contains 400-800
cells, with extremely thin walls and scanty cytoplasm (fig. 23). The
only differentiation observable is the abundant accumulation of
reserve food in the peripheral cells of the antipodal region. The
whole mass of endosperm at this period usually measures 20 by 30/4 ;
while in the mature seed the endosperm mass is ordinarily about
20 mm i on g ky j^mm at j ts w id es t p ar t ? an d all of it surcharged with
starch and other food materials. The food material is particularly
conspicuous in a broad central band extending from the advancing
tip of the embryo and widening to the antipodal end of the sac. Fig.
5 shows the longitudinal extent of the band, and fig. 4 its cross-section.
The peculiar behavior of the endosperm after fertilization will be
considered under the discussion of the maturing of the seed.
The forcible discharge of the contents of the tube may be inferred
from the vacuole-like appearance in the center of the egg, produced
by the inrush (figs. 24 and 25). The male nucleus in its cytoplasmic
sheath passes through the cytoplasm of the egg and comes in contact
with the egg nucleus. The male cytoplasm becomes closely appressed
170 BOTANICAL GAZETTE [march
to the surface of the female nucleus, slips from its own nucleus, and
was observed extending over fully two-thirds of the female nucleus
(fig. 24). This behavior of the male cytoplasm has been observed
by Coker (3) in Taxodium and by Miss Robertson (9) in Torreya
calijomica. The male cytoplasm of Torreya taxifolia is sharply
differentiated by staining from the cytoplasm of the egg, and undoubt-
edly completely invests the fusion nucleus. The appearance of a
similar mass of cytoplasm investing the free nuclei of the first division
(fig. 25), and continued in the second division in connection with
wall-formation (fig. 26) suggests the possibility that the male cyto-
plasm may remain differentiated through more than one cell genera-
tion. Near the neck end of the archegonium nuclei are evident,
which seem to be the stalk and tube nuclei and the other male nucleus
with its investing cytoplasm (fig. 24).
Soon after fertilization the first division of the egg nucleus was
observed (fig. 25), and almost immediately the second division fol-
lows, giving rise to four large free nuclei almost filling the egg (fig.
26), one nucleus in the base of the egg, the other three in a plane
above. At this time wall-formation occurs, the cytoplasmic radiations
which precede it being very evident (fig. 26). Two weeks later the
egg is completely filled with a proembryo consisting of twelve to
eighteen cells (fig. 27). This complete filling of the egg by the pro-
embryo is remarkable among Coniferales, having recently been
observed also by Lawson (4) in Sequoia, but as yet not recorded
in other genera. In Torreya, at least, this fact seems to be related
to the relatively small size of the egg, the very large nuclei, and the
early appearance of walls.
The cells of the proembryo at this early stage are distinctly in three
tiers; that nearest the neck of the archegonium comprising five or six
cells and forming the primary suspensor tier; the middle tier, com-
prising five or six cells and forming the secondary suspensor tier; and
the lowest consisting of a single cell which ultimately contributes to
suspensor-formation and forms the embryo. The inequality in the
number of cells entering into the tiers seems to be characteristic of
Taxaceae. In Podocarpus Coker (2) found the three tiers made up
1905] COULTER 6-= LAND—TORREYA TAXI FOLIA 171
of eleven cells in each of the upper two and one in the lowest; and a
similar but less striking inequality is to be observed in Taxus. Occa-
sionally in Torreya other divisions may occur, giving rise to approxi-
mately four tiers and a proembryo of about eighteen cells; but no
other division occurs until the following spring, the winter condition
being a proembryo of three or four tiers of cells as described above.
In the following season the suspensor develops and the embryo
is formed, along with the characteristic " rumination" of the endo-
sperm and the development of the testa. The first indication of
change from the winter proembryonic condition is the elongation of
the primary suspensor cells (fig. 29); a little later this is shared by
the secondary suspensor cells; and this is followed by the elongation
of the third tier, if four tiers are formed. In the meantime the termi-
nal cell has begun a series of rapid divisions, resulting in a cylindrical
mass of meristematic tissue, much as Lyon (5) has described in the
case of the embryo of Ginkgo. This meristematic cylinder advances
gradually into the endosperm, its basal tiers of cells successively
contributing to the suspensor elongation. Thus in the formation
of the suspensor there seems to be developed what may be called a
wave of elongation, beginning with the uppermost tier of the pro-
embryo and extending gradually downward, tier after tier, until it
includes the upper region of the meristematic cylinder formed by
the terminal cell. This same phenomenon is very evident also in
After the meristematic cylinder has advanced into the endosperm
and has become prominent, the growing points are organized; the
two cotyledons presently becoming beautifully crescentic in outline
and completely surrounding the stem- tip; and the root-tip being
organized deep within the meristematic cylinder.
In several instances a number of small embryos were observed
imbedded in the endosperm about the suspensor region of the normal
embryo. Our material did not permit any determination of their
origin, but they resemble the proembryo of the normal embryo, and
are developed while the latter is in its second season's growth. After
the pollen tube has reached the archegonium, the endosperm grows
up around it (figs. 23 and 24), so that the tube lies in a cup-shaped
depression. After fertilization, the rim of this endosperm cup con-
172 BOTANICAL GAZETTE [march
tinues growth and gradually incloses trie fertilized egg, in most cases
forming quite an elongated beak above the embryo. Later many
of these cells round off, forming a loose tissue, and it is among these
rounded-off cells that the feeble accessory embryos are produced.
Whether these have been developed apogamously from the endosperm
cells, or have budded from the suspensor cells can only be conjectured.
In any event, they might develop further if there was any failure in
the development of the normal embryo.
The time involved in the series described above, that is from the
first appearance of the megasporangiate strobilus to the maturity of
the seed, is about thirty months, distributed as follows: June (?),
first appearance of the strobilus; April, mother- cells in synapsis;
August, fertilization; October, proembryo of 12 to 18 cells (winter
condition); following season, development of embryo, " rumination"
of endosperm, and development of testa; October, fall of seed.
MATURING OF SEED.
The outer integument and its histological continuation about the
ovule develops a thick fleshy coat containing very numerous large
resin cavities, and completely inclosing the structures within (figs.
4 and 5). This fleshy coat gives to the mature seed the appearance
of a plum (fig. 3), as in the seeds of Cycads and Ginkgo. Within
the broad band of resin cavities, near the inner limit of the integu-
ment, two conspicuous vascular strands occur, directly opposite one
another (fig. 4). These are the main strands of the very character-
istic vascular system of the ovule described by Oliver (7).
The inner integument early differentiates into two distinct layers,
a differentiation just as evident in Cycads and Ginkgo. The outer
layer forms the stony coat, and the transformation from soft to very
hard tissue begins after the embryo and endosperm have completed
their development. The hardening begins at the apex of the ovule,
and on account of resistance to stains appears under low power as a
clear band (black in fig. 5). The hardening band gradually extends
downwards through the relatively very short integument, and differ-
entiating as a distinct layer in the much larger mass of tissue below
completely invests the ovule within the fleshy coat. Protoplasmic
connections between the cells of the stony coat and striations in the
cell walls are unusually clear.
1905] COULTER &> LAND—TORREYA TAXIFOLIA 173
The inner layer of the inner integument comprises several layers
of thin- walled cells, but beyond the integuments it is not histologically
differentiated as a layer distinct from the tissue within. Accordingly,
through the great bulk of the seed this layer may be neglected, and
the whole mass of tissue within the stony layer and outside of the
embryo sac will be spoken of as nuclear tissue or perisperm.
The behavior of the endosperm is peculiar, resulting in what is
called " ruminated endosperm," a phenomenon peculiar to Torreya
among gymnosperms, and commonly illustrated by the nutmeg
" Rumination" of endosperm proves to be a misnomer, for the endo-
sperm is always the successfully aggressive tissue in developing this
condition. The perisperm continues to grow throughout the matur-
ing of the seed, and the final condition results from what might be
called the struggle of two growing tissues that have been abutting upon
one another through their whole period of growth.
In ordinary seeds the endosperm invades the surrounding tissue
more or less uniformly; in the case of Cycads and Ginkgo, for exam-
ple, obliterating most of the perisperm. In Torreya, on the other
hand, the invasion by the endosperm is irregular in the extreme.
It is in the season after the proembryo has been formed that the active
invasion of the perisperm begins. The extension of the endosperm
into the tip of the nucellus above the sac proceeds in the usual way,
obliterating all of it except a few peripheral layers of cells. This uni-
form invasion seems to be due to the fact that in this apical region
(the original nucellus) the perisperm is not growing actively if at all.
Below this small region at the tip, however, the perisperm is very active
and evidently resists disintegration much more at certain points than
at others. As a consequence, the perisperm becomes eroded by the
irregularly advancing endosperm, and is left in the condition of a much
dissected coast-line (figs. 4 and 5). To the casual observer this results
in an appearance suggesting that the endosperm is being invaded by
plates of perisperm, but this is no more true than that the promontories
of a dissected coast-line are advancing into the sea. The suggestion of
an invading perisperm is further strengthened by the fact that within
the perisperm bordering the endosperm a dark brown and finally
black band of cells is developed, due to abundant food storage (figs.
4, 30, 31), but this really recedes as the endosperm advances.
174 BOTANICAL GAZETTE [march
A cross-section of the mature seed always shows a definite and deep
constriction of the endosperm in the center, exactly opposite the two
opposed vascular strands that run up on each side of the seed through
the inner part of the outer integument (fig. 4). This constriction is
the cross-section of two opposite and deep longitudinal furrows in the
endosperm, and it means that in this longitudinal plane the endosperm
encounters the greatest resistance in invading the perisperm. This
most resistant perisperm certainly seems to hold a very definite topo-
graphical relation to the principal vascular strands, and this relation
may explain the resistance.
That endosperm is the aggressive tissue at every point, even at
the region of most resistant perisperm, is evident for several reasons.
In no case were the peripheral cells of the endosperm broken down;
and in no case did there fail to appear one or two layers of disorgan-
ized cells of the perisperm in contact with the endosperm (figs. 30
and 31). In every case, also, the peripheral cells of the endosperm
appeared active and very vigorous, and their different appearance in
regions of more and less active encroachment is striking. In regions
of active invasion the endosperm cells are radially elongated, and
many of them are binucleate (fig. 30) ; while in regions of less active
invasion the cells are more nearly isodiametric and rarely binucleate
Another proof that endosperm is the encroaching tissue may be
obtained from comparative measurements. At the times of fertili-
zation the gametophyte usually measures 20 by 30/x. In the mature
seed the ordinary length of the gametophyte is 20 mm , the greatest
width being i4 mm , and the least (at the deep constriction opposite
the vascular strands)) i.5 mm . At this most resistant region of the
perisperm, therefore, where it is hard to escape the conviction that
the perisperm plate has cut the endosperm nearly in two, the endo-
sperm has increased its diameter against the perisperm seventy-five
The best reason, however, for concluding that the endosperm is
the invading tissue in this case is that this is always the behavior of
endosperm; and it is singular that the old explanation of " rumination' '
was ever suggested. An examination of the nutmeg, the classic
illustration of " ruminated endosperm/ ' and of Asimina triloba,
1905] COULTER & LAND—TORREYA TAXIFOLIA 175
showed that precisely the same explanation applies to them that we
have given in the case of Torreya.
The staminate strobilus consists of a series of closely overlapping
sterile bracts, in four vertical rows, completely enveloping the tip of
the axis bearing numerous stamens. The large adaxial resin cavity
that occurs in the stamen occupies the site of three abortive sporangia.
The male gametophyte has no prothallial cell, and the male cells
are very unequal, resembling those of Taxus. The pollen tube is
exceedingly variable in the rate and direction of its advance through
the nucellar cap, sometimes pushing in the embryo sac while it is
in an early free-nucleate stage.
The ovulate strobilus consists of four enveloping bracts and a
single terminal ovule with two integuments. Extensive intercalary
growth below the mother-cell forms the bulk of the mature ovule
and seed. There is no organization of a special digestive layer
around the mother-cell.
The solitary archegonium initial appears as soon as walls are
formed, is always at one side of the central axis of the gametophyte,
and forms a two-celled neck. The nucleus of the central cell was
not observed to divide, nor could any trace of a ventral nucleus be
In fertilization the male cytoplasm invests the fusion nucleus,
and seems to remain distinct until wall-formation at the four-
nucleate stage of the proembryo.
In the development of the proembryo, four free nuclei appear
before wall-formation, and the proembryo completely fills the egg,
having no "open cells.' ' A proembryo of twelve to eighteen cells
is the winter stage. In the spring the suspensor is formed by what
may be called a wave of elongation, beginning with the uppermost
tier of the proembryo, and extending gradually downward, tier after
tier, until it includes the upper region of the meristematic cylinder
formed by the terminal cell.
Small embryos are formed during the second season in the sus-
pensor region of the normal embryo; but whether they arise from
prothallial or suspensor cells was not determined.
176 BOTANICAL GAZETTE [march
The "rumination" of endosperm, peculiar to Torreya among
gymnosperms, arises from the extremely irregular encroachment of
the endosperm upon the perisperm, the endosperm being resisted
much more at certain points than at others. The same was found
to be true of other "ruminated" seeds.
The University of Chicago.
1. Chapman, A. W., Torreya taxijolia Arnott; a reminiscence. Bot. Gazette
10:251-254. map. 1885.
2. Coker, W. C, Notes on the gametophytes and embryo of Podocarpus.
Bot. Gazette 33:89-107. pis. 5-7. 1902.
3. , On the gametophytes and embryo of Taxodium. Bot. Gazette
36:1-27, 114-140. pis. i-ii. 1903.
4. Lawson, A. A., The gametophytes, archegonia, fertilization, and embryo of
Sequoia sempervirens. Ann. Botany 18:1-28. pis. 1-4. 1904.
5. Lyon, H. L., The embryogeny of Ginkgo. Minn. Bot. Studies 3:275-290.
pis. 29-43. 1904.
6. Oliver, F. W., On some points of apparent resemblance in certain fossil
and recent gymnospermous seeds. New Phytologist 1 : 145-154. 1902.
7. , The ovules of the older gymnosperms. Ann. Botany 17:451-476.
pi. 24. 1903.
8. Robertson, Agnes, Spore formation in Torreya calif ornica. New Phytolo-
gist 3:133-148. pis. 3~4- 1904.
9. — , Studies in the morphology of Torreya calif ornica Torr. II. The
sexual organs and fertilization. New Phytologist 3:205-216. pis. y-g.
10. Strasburger, E., Anlage des Embryosackes und Prothalliumbildung bei
der Eibe nebst anschliessenden Erorterungen. Festschrift Ernst Haeckel.
EXPLANATION OF PLATES I-IV.
With the exception of Plate 7, all figures were drawn with the aid of an Abbe
camera lucida and reduced one-half in reproduction. Abbreviations are as
follows: br, bract; a, primordium of stamen; oi, outer integument; ii, inner
integument; r, resin cavity; n, nucellus; pc, pollen chamber; s, sporogenous
cells; tn, tube nucleus; g, primary spermatogenous cell; stn, nucleus of stalk
cell; b, body cell; Wi functional male cell; m 2 functionless male cell; hr, haus-
torial region of female gametophyte; nc, nucleus of neck cell; 0, egg; end, endo-
sperm; per, perisperm.
1905] COULTER & LAND—TORREYA TAXIFOLIA 177
Fig. 1. Staminate branch; October 21, 1904. Xi.
Fig. 2. Ovulate branch; April 7, 1904. Xi.
Fig. 3. Mature seed; October 21, 1904. Xi.
Fig. 4. Cross-section of seed showing ruminated endosperm with storage
region in center, seed coats, stored food in the perisperm, and resin ducts. X3.
Fig. 5. Longitudinal median section through seed showing embryo, rumi-
nated endosperm, and seed coats. X3.
Fig. 6. Transverse section through a staminate strobilus showing bracts and
primordia of stamens; August 12, 1904. X24.
Fig. 7. Longitudinal section through a staminate strobilus showing envelop-
ing bracts, primordia of stamens, and storage region; the position of the bundles
is shown by the dotted lines; August 12, 1904. X24.
Fig. 8. Primordium of a stamen; August 12, 1904. X460.
Fig. 9. Median section through an adaxial sporangium showing the disor-
ganizing primary sporogenous cell and two wall cells; October 21, 1904. X460.
Fig. 10. Cross-section of a sporophyll showing the three abortive adaxial
and the three functional abaxial sporangia; October 21, 1904. X47.
Fig. 11. Longitudinal section through a stamen showing early stage of the
resin cavity above and a functioning sporangium below; October 21, 1904. X 255.
Fig. 12. Pollen grain showing primary spermatogenous cell and tube cell;
April 7, 1904. X1250.
Fig. 13. Tip of a pollen tube which has penetrated about half way through
the nucellus; June 10, 1904. X460.
Fig. 14. Tip of pollen tube in contact with the embryo sac; the female garnet -
ophyte is in the free nuclear stage and the nuclei are placed parietally; June 21,
Fig. 15. Embryo sac in free nuclear stage showing one of the nuclei occupy-
ing the place of the megaspore mother-cell; June 10, 1904. X185.
Fig. 16. Pollen tube in contact with the endosperm; an archegonium is at
the left of the tube; July 26, 1904. X255.
Fig. 17. Young ovulate strobilus showing enveloping bracts, inner integu-
ment, and nucellus; July 26, 1904. X47.
Fig. 18. Ovulate strobilus showing bracts, integuments, nucellus with rudi-
mentary pollen chamber, and megaspore mother-cell; April 7, 1904. X24.
Fig. 19. Tip of nucellus with pollen chamber containing a microspore;
April 8, 1904. X220.
Fig. 20. Megaspore mother-cell in synapsis; April 7, 1904. X460.
Fig. 21. Micropylar end of female gametophyte with archegonium initial
projecting into the space formerly occupied by the megaspore mother-cell; July
26, 1904. X460.
178 BOTANICAL GAZETTE [march
Fig. 22. Archegonium consisting of two neck cells and central cell; the
nucleus of the central cell has rounded out, and is passing downward to the center
of the cell and taking on the appearance of an egg nucleus; July 26, 1904. X460.
Fig. 23. Median longitudinal section of female gametophyte showing egg,
remains of a neck cell, and antipodal haustorial cells; the tip of the pollen tube
in contact with the egg contains stalk and tube nuclei, functional and functionless
male cells; the upward growth of the endosperm cells forms a sheath around
the pollen tube; August 12, 1904. X460.
Fig. 24. Fertilization; the male nucleus is in contact with the egg nucleus;
the cytoplasm of the male cell is closely applied to the egg nucleus; the function-
less male cell, and tube and stalk nuclei are in the upper part of the egg cytoplasm;
the cavity in the egg cytoplasm is caused by the inrush of the contents of the
pollen tube; August 12, 1904. X460.
Fig. 25. Two-celled proembryo; the dense cytoplasmic mass surrounding
the nuclei is probably in greater part derived from the male cytoplasm; August
27, 1904. X460.
Fig. 26. Four-celled proembryo; walls coming in; August 12, 1904. X460.
Fig. 27. Proembryo shortly after walls are laid down; the proembryo passes
the winter in this stage; August 27, 1904. X460.
Fig. 28. Cross-section through suspensor cells; September 12, 1904. X460.
Fig. 29. Proembryo showing elongation of suspensor cells; April 7, 1904.
Fig. 30. Endosperm cells encroaching on perisperm; August 12, 1904. X640.
Fig. 31. Endosperm cells which have ceased to encroach on perisperm;
August 12, 1904. X460.
BOTANICAL GAZETTE, XXXIX
COULTER & LAND on TORREYA.
BOTANICAL GAZETTE, XXXIX
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